Arbuscular mycorrhizal fungal hyphae reduce soil erosion by surface
water flow in a greenhouse experiment
Mardhiah , U., Caruso, T., Gurnell, A., & Rillig, M. C. (2016). Arbuscular mycorrhizal fungal hyphae reduce soil
erosion by surface water flow in a greenhouse experiment. Applied Soil Ecology, 99, 137-140. DOI:
10.1016/j.apsoil.2015.11.027
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Applied Soil Ecology
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Download date:15. Jun. 2017
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Arbuscular mycorrhizal fungal hyphae reduce soil erosion by surface water flow in
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a greenhouse experiment
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Ulfah Mardhiah1,2*, Tancredi Caruso3, Angela Gurnell4, Matthias C. Rillig1,2
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Berlin, Germany
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Berlin, Germany
Freie Universität Berlin, Institut für Biologie, Plant Ecology, Altensteinstr. 6, D-14195,
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), D-14195
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Food Security, 97 Lisburn Road, BT9 7BL, Belfast, Northern Ireland, United Kingdom
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London, United Kingdom
Queen’s University of Belfast, School of Biological Sciences and Institute for Global
Queen Mary, University of London, School of Geography, Mile End Road, E1 4NS,
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*Corresponding author
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Ulfah Mardhiah, Freie Universität Berlin, Institut für Biologie, Plant Ecology,
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Altensteinstr. 6, D-14195, Berlin, Germany
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Tel ++49 30 838 53143; fax – 53886; [email protected]
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Abstract
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The role of arbuscular mycorrhizal fungi (AMF) in resisting surface flow soil erosion has
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never been tested experimentally. We set up a full factorial greenhouse experiment using
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Achillea millefolium with treatments consisting of addition of AMF inoculum and non-
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microbial filtrate, non-AMF inoculum and microbial filtrate, AMF inoculum and
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microbial filtrate, and non-AMF inoculum and non-microbial filtrate (control) which
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were subjected to a constant shear stress in the form of surface water flow to quantify the
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soil detachment rate through time. We found that soil loss can be explained by the
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combined effect of roots and AMF extraradical hyphae and we could disentangle the
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unique effect of AMF hyphal length, which significantly reduced soil loss, highlighting
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their potential importance in riparian systems.
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Keywords: Soil erosion, concentrated flow, soil detachment rate, AMF
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The rate of soil loss by erosion has been accelerated due to various human activities at a
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global scale (Grimm et al., 2002), with negative effects including loss of topsoil, decrease
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in soil organic matter, and pollution of surface waters (Lal, 2001). Soil erosion is related
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to the susceptibility of soil to both detachment and transport of soil particles (Gyssels et
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al., 2005). Vegetation biomass, both above and belowground, has been identified to play a
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role in decreasing soil erosion (Prosser et al., 1995; Gyssels and Poesen, 2003). The role
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of soil biota has not often been subjected to empirical tests, but it is assumed that
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members of the soil biota indirectly decrease soil erosion through the formation and
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stabilization of soil aggregates (Tisdall and Oades, 1982; Rillig and Mummey, 2006). For
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example, arbuscular mycorrhizal fungi (AMF) are root associated fungi known for their
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role in increasing soil aggregation (Tisdall and Oades, 1982; Mardhiah et al., 2014;
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Leifheit et al., 2014) through their extended extraradical hyphae in the rhizosphere
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(Tisdall and Oades, 1982; Rillig and Mummey, 2006) and by stimulating root growth
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(Bearden and Petersen, 2000).
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In order to quantify the role of AMF hyphae in reducing soil erosion, we measured at the
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end of a greenhouse experiment the difference in soil detachment rate (g soil 10 s-1) under
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a constant flow of water across a fixed area of soil surface (63.6 cm2) at successive points
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in time, comparing different treatments (AMF treatment, microbial filtrate treatment,
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AMF and microbial filtrate treatment and control). Achillea millefolium seeds were
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surface sterilized in 70% ethanol and 5% commercial bleach. We added 5 seeds per pot
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and then thinned to two plants per pot. We used a sandy loam alluvial soil (73% sand,
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18% silt and 7% clay (Rillig et al., 2010)), which was autoclaved twice (121°C, 20
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minutes) and was re-mixed before placing into each pot (1.3 kg of soil per pot). Pots in
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AMF treatments received 150 Glomus intraradices (Rhizophagus irregularis) spores;
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non-AMF treatment pots received the same amount of sterile carrier material. We
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prepared the microbial filtrate, which might introduce saprobic fungi and bacteria, by
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passing a suspension of the soil used in the study (200 g L-1) through a 20 μm size sieve
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and used the slurry as microbial filtrate treatment. Pots in microbial filtrate treatments
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received 2 ml of the slurry, while those in non-microbial filtrate treatment received the
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same amount of sterile slurry. The greenhouse temperature was 16-22°C and the
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experiment lasted for ~ 23 weeks. The plants were of similar size by the end of the
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experiment.
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To measure the soil erosion due to water flowing over the soil surface, a hydraulic flume,
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2 m in length and 0.1 m wide, was constructed using a transparent Plexi glass wall at the
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University of Trento, Italy. At 20 cm before the end of the flume, a hole with a 9 cm
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external diameter was created to hold the soil core. A sharpened PVC pipe (inner
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diameter = 9 cm), made to fit the flume hole, was used as a corer and was carefully
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placed at the centre of each of the pots and pushed through the soil from the top until it
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reached the bottom of each pot. The corer was then pushed through from below and
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towards the surface of the flume bottom using a piston so that the soil surface was
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maintained in line with the flume bed through each experiment (Suppl. Mat. Figure S1).
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The flume was set at a slope of 18°, and a flow of tap water was discharged into the flume
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at a constant rate (0.0003 m3 s-1). Mean flow velocity (1.17 ± 0.01 m s-1) was measured
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every day and yielded a mean flow shear stress on the soil surface of 7.75 Pa (Suppl. Mat.
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Equation S1).
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Ten replicate samples were prepared according to each treatment. Samples were prepared
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with methods adjusted from De Baets et al. (2006). The samples were retained within a
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constant water level environment (4.5 cm below the soil surface) to allow slow capillary
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rise and all aboveground biomass was clipped. The samples were drained immediately
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prior to being introduced to the flume, where they were subjected to a constant discharge
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for 145 seconds. Following an initial flow period of 20 seconds, samples of the water
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draining from the flume were taken every 15 seconds for 10 seconds, providing a total of
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five successive 10 second samples (R1-R5). The samples were left to settle before
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decanting the water, which was oven dried at 65°C and then the residue was weighed.
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Soil which was left in the corer was carefully retained and dried. To ensure that
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measurements of the soil left in the corer did not include soil and roots exposed by the
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soil erosion experiment, we carefully scraped a thin layer of the surface layer off each
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cored soil. After sieving the soil through a 4-mm sieve, aggregate stability was measured
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by re-wetting 4.0 g of soil using capillary action and sieving for 5 minutes on a 250 μm
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sieve before drying at 65°C. The dried material was then crushed and passed through the
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sieve, separating the stable aggregates from the coarse fraction. Root biomass was
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extracted and measured using an extraction-flotation method (Cook et al., 1988). Root
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length grouped by diameter (Barto et al., 2010) was measured by analyzing scanned
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images using WinRhizo Pro 2007d (Regent Instruments Inc., Quebec City, Canada).
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Hyphae were extracted from 4.0 grams of dried soil using a protocol adapted from
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Jakobsen et al. (1992) and then stained with Trypan Blue. AMF and non-AMF
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extraradical hyphal length were measured according to Rillig et al. (1999).
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We used the Kruskal Wallis test to quantify the difference of soil detachment rate (g soil
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10 s-1) between treatments at each of the five successive time points during the flume
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experiments. We also ran linear models correlating total soil loss with soil detachment
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rate determinants (percent water stable aggregates (% WSA), root biomass, very fine, fine
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and coarse root length, AMF and non-AMF extraradical hyphal length) tested as main
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effect and interaction. We calculated variation in partitioning of root biomass and AMF
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extraradical hyphal length using redundancy analysis. All statistical analyses were
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conducted using version 2.14.0 of the R statistics software (R Development Core Team,
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2012).
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In general, soil loss decreased through time (Suppl. Mat. Figure S2). A possible
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explanation is that initially, relatively loose surface soil which came into contact with the
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erosion flow was rapidly detached; soil loss then slowed, possibly because of more
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intense effects of roots with or without fungal hyphae. We found that AMF treatments
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decreased soil loss most effectively compared to the control (Figure 1). Total soil loss can
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be explained by the joint effect of total root biomass (17%) and AMF extraradical hyphae
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(16%) (Table 1). AMF extraradical hyphal length significantly decreased total soil loss
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when used in linear models as a singular main effect and in interaction with root biomass
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(Suppl. Mat. Table S1, Figure 2). This is to our knowledge, the first time that AMF
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extraradical hyphal length has been shown to have a direct effect in reducing surface soil
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erosion due to surface flow. The role of AMF seems to be due to the ability of AMF to
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produce extraradical hyphae. The addition of microbial filtrate did not reduce the soil
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detachment rate compared to the control and even reduced the effectiveness of AMF
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treatment. We also did not find a significant difference of %WSA between treatments
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(Suppl. Mat. Table S3) and no significant correlations between the soil detachment rate
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and % WSA in our models (data not shown). This implies that soil aggregate stability in
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our system was not an important factor for preventing soil erosion due to concentrated
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flow. Studies showed that besides soil aggregates, microtopography (surface roughness)
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and soil cohesion due to a dense root mat, can decrease surface soil erosion (Campbell
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et.al., 1989; Prosser et al., 1995; Prosser and Dietrich, 1995; Hu et al., 2002). Our study
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implies that, rather than the role in formation or maintenance of stable soil aggregates, the
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role of AMF hyphae -which might also include the formation of a hyphal network which
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further increases soil cohesion- might be more important in reducing surface soil erosion.
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Although the microbial filtrate might contain saprobic fungi which also produced hyphae,
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their minimal effect towards reduced soil erosion in this study might imply that the
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hyphae of both fungal groups behave differently. AMF tend to produce more persistent,
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coarser and thicker extraradical hyphae compared to many saprobic fungal hyphae
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(Klironomos and Kendrick, 1996; Klironomos et al., 1999; Allen, 2006). Saprobic fungi
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can also produce enzymes degrading soil carbon, an ability which AMF lack; this taken
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together could explain the significant role of AMF in reducing soil erosion in our
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experiment. Overall, our results highlight the role of AMF in potentially stabilizing soils
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in riparian systems.
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Acknowledgments
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This research was funded by the SMART Joint Doctoral Programme (Erasmus Mundus
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Programme of the European Union) and the DRS HONORS Fellowship programme of
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Freie Universität Berlin. This study is a contribution to an EU Marie Curie Career
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Integration Grant to T.C. (EC FP7 - 631399 - SENSE). We would like to thank Dr. Walter
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Bertoldi and Dr. Marco Redolfi for providing the flume and for invaluable discussion on
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the flume experiment. We would also like to thank the two anonymous reviewers for their
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invaluable input and comments.
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Table 1. Variation partitioning based on redundancy analysis was used to explain the
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pattern of total soil loss in relation to explanatory variables: AMF extraradical hyphal
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length and root biomass. All percentages explained were significant (p-values < 0.05).
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Response variable:
Total soil loss (g soil in 50 s)
Explanatory variables:
AMF extraradical hyphal length fraction
(with covariable: root biomass)
Root biomass fraction
(with covariable: AMF extraradical hyphal length)
Total
Shared fraction
Residuals
AMF extraradical hyphal length (without covariable)
Root biomass (without covariable)
df
Fraction explained (%)
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1
17
2
0
1
1
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4.1
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9.7
10.2
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Figure captions
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Figure 1. Linear models fitted using the generalized least squares (GLS) method
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corrected for heterogeneity of variances (var = varIdent(form=~1|fcategorical)) were used
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to plot cumulative soil detachment rate through time (R1, R2, R3, R4, R5) for different
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treatments (“control”, “AMF treatment”, “AMF and microbial filtrate treatment” and
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“microbial filtrate treatment”). Figure shows fitted lines with significant differences
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between each treatment levels (Suppl. Mat. Table S2). Different symbols indicate
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different treatments (control = ∆, AMF treatment = ●, AMF and microbial filtrate
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treatment = ○, microbial filtrate treatment = +). The highest data point (microbial filtrate
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treatment, ranging 12.15-30.03 g soil 10 s-1, R1-R5) was omitted to enable clear
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visualization of data.
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Figure 2. A linear model fitted using the generalized least square (GLS) method corrected
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for heterogeneity of variances (var = varIdent(form=~1|fcategorical)) and spatial
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autocorrelation was used to correlate total soil loss (y axis) to AMF extraradical hyphal
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length (x axis).
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